Impact of Endemic Besnoitiosis on the Performance of a Dairy Cattle Herd
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Herd Description and Study Area
2.2. Sampling and Data Collection
2.3. Indirect Fluorescent Antibody Test
2.4. Clinical Examination
2.5. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Álvarez-García, G.; Frey, C.F.; Mora, L.M.O.; Schares, G. A Century of Bovine Besnoitiosis: An Unknown Disease Re-Emerging in Europe. Trends Parasitol. 2013, 29, 407–415. [Google Scholar] [CrossRef] [PubMed]
- Diesing, L.; Heydorn, A.O.; Matuschka, F.R.; Bauer, C.; Pipano, E.; de Waal, D.T.; Potgieter, F.T. Besnoitia Besnoiti: Studies on the Definitive Host and Experimental Infections in Cattle. Parasitol. Res. 1988, 75, 114–117. [Google Scholar] [CrossRef] [PubMed]
- Basso, W.; Schares, G.; Gollnick, N.S.; Rütten, M.; Deplazes, P. Exploring the Life Cycle of Besnoitia Besnoiti-Experimental Infection of Putative Definitive and Intermediate Host Species. Vet. Parasitol. 2011, 178, 223–234. [Google Scholar] [CrossRef] [PubMed]
- Seltmann, A.; Schares, G.; Aschenborn, O.H.K.; Heinrich, S.K.; Thalwitzer, S.; Wachter, B.; Czirják, G.A. Species-Specific Differences in Toxoplasma Gondii, Neospora Caninum and Besnoitia Besnoiti Seroprevalence in Namibian Wildlife. Parasites Vectors 2020, 13, 7. [Google Scholar] [CrossRef] [PubMed]
- González-Barrio, D.; Köster, P.C.; Habela, M.A.; Martín-Pérez, M.; Fernández-García, J.L.; Balseiro, A.; Barral, M.; Nájera, F.; Figueiredo, A.M.; Palacios, M.J.; et al. Molecular Survey of Besnoitia Spp. (Apicomplexa) in Faeces from European Wild Mesocarnivores in Spain. Transbound. Emerg. Dis. 2021, 68, 3156–3166. [Google Scholar] [CrossRef]
- Gutiérrez-Expósito, D.; Ferre, I.; Ortega-Mora, L.M.; Álvarez-García, G. Advances in the Diagnosis of Bovine Besnoitiosis: Current Options and Applications for Control. Int. J. Parasitol. 2017, 47, 737–751. [Google Scholar] [CrossRef]
- Bigalke, R.D. New Concepts on the Epidemiological Features of Bovine Besnoitiosis as Determined by Laboratory and Field Investigations. Onderstepoort J. Vet. Res. 1968, 35, 3–138. [Google Scholar]
- Cortes, H.C.E.; Reis, Y.; Waap, H.; Vidal, R.; Soares, H.; Marques, I.; Pereira da Fonseca, I.; Fazendeiro, I.; Ferreira, M.L.; Caeiro, V.; et al. Isolation of Besnoitia Besnoiti from Infected Cattle in Portugal. Vet. Parasitol. 2006, 141, 226–233. [Google Scholar] [CrossRef]
- Liénard, E.; Salem, A.; Grisez, C.; Prévot, F.; Bergeaud, J.P.; Franc, M.; Gottstein, B.; Alzieu, J.P.; Lagalisse, Y.; Jacquiet, P. A Longitudinal Study of Besnoitia Besnoiti Infections and Seasonal Abundance of Stomoxys Calcitrans in a Dairy Cattle Farm of Southwest France. Vet. Parasitol. 2011, 177, 20–27. [Google Scholar] [CrossRef]
- Fernández-García, A.; Alvarez-García, G.; Risco-Castillo, V.; Aguado-Martínez, A.; Marcén, J.M.; Rojo-Montejo, S.; Castillo, J.A.; Ortega-Mora, L.M. Development and Use of an Indirect ELISA in an Outbreak of Bovine Besnoitiosis in Spain. Vet. Rec. 2010, 166, 818–822. [Google Scholar] [CrossRef]
- Sharif, S.; Jacquiet, P.; Prevot, F.; Grisez, C.; Raymond-Letron, I.; Semin, M.O.; Geffré, A.; Trumel, C.; Franc, M.; Bouhsira, E.; et al. Stomoxys Calcitrans, Mechanical Vector of Virulent Besnoitia Besnoiti from Chronically Infected Cattle to Susceptible Rabbit. Med. Vet. Entomol. 2019, 33, 247–255. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cortes, H.; Leitão, A.; Gottstein, B.; Hemphill, A. A Review on Bovine Besnoitiosis: A Disease with Economic Impact in Herd Health Management, Caused by Besnoitia Besnoiti (Franco and Borges). Parasitology 2014, 141, 1406–1417. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- EFSA. Bovine Besnoitiosis: An Emerging Disease in Europe. EFSA J. 2010, 8, 1499. [Google Scholar] [CrossRef]
- Hornok, S.; Fedák, A.; Baska, F.; Hofmann-Lehmann, R.; Basso, W. Bovine Besnoitiosis Emerging in Central-Eastern Europe, Hungary. Parasites Vectors 2014, 7, 20. [Google Scholar] [CrossRef] [Green Version]
- Gazzonis, A.L.; Garcia, G.A.; Zanzani, S.A.; Garippa, G.; Rossi, L.; Maggiora, M.; Dini, V.; Invernizzi, A.; Luini, M.; Tranquillo, V.M.; et al. Besnoitia Besnoiti among Cattle in Insular and Northwestern Italy: Endemic Infection or Isolated Outbreaks? Parasites Vectors 2014, 7, 585. [Google Scholar] [CrossRef]
- Vanhoudt, A.; Pardon, B.; De Schutter, P.; Bosseler, L.; Sarre, C.; Vercruysse, J.; Deprez, P. First Confirmed Case of Bovine Besnoitiosis in an Imported Bull in Belgium. Vlaams Diergeneeskd. Tijdschr. 2015, 84, 205–211. [Google Scholar] [CrossRef]
- Ryan, E.G.; Lee, A.; Carty, C.; O’Shaughnessy, J.; Kelly, P.; Cassidy, J.P.; Sheehan, M.; Johnson, A.; De Waal, T. Bovine Besnoitiosis (Besnoitia Besnoiti) in an Irish Dairy Herd. Vet. Rec. 2016, 178, 608. [Google Scholar] [CrossRef]
- Waap, H.; Nunes, T.; Cortes, H.; Leitão, A.; Vaz, Y. Percepção Da Besnoitiose Bovina Em Portugal—Questionário Aos Médicos Veterinários de Campo. Rev. Port. Ciências Veterinárias 2015, 110, 201–208. [Google Scholar]
- Cortes, H.; Chagas e Silva, J.; Baptista, M.C.; Pereira, R.M.; Leitão, A.; Horta, E.M.; Vasques, M.I.; Barbas, J.P.; Marques, C.C. Besnoitia besnoiti impact on fertility of cattle exploited in Mediterranean pastures (Alentejo). In Animal Products from the Mediterranean Area; Ramalho Ribeiro, J.M.C., Horta, A.E.M., Mosconi, C., Rosati, A., Eds.; Wageningen Academic Publishers: Wageningen, The Netherlands, 2006; pp. 323–329. [Google Scholar]
- Grau-Roma, L.; Martínez, J.; Esteban-Gil, A.; López, J.; Marco, A.; Majó, N.; Castillo, J.A.; Domingo, M. Pathological Findings in Genital Organs of Bulls Naturally Infected with Besnoitia Besnoiti. Parasitol. Res. 2020, 119, 2257–2262. [Google Scholar] [CrossRef]
- Jacquiet, P.; Liénard, E.; Franc, M. Bovine Besnoitiosis: Epidemiological and Clinical Aspects. Vet. Parasitol. 2010, 174, 30–36. [Google Scholar] [CrossRef]
- Villa, L.; Gazzonis, A.L.; Zanzani, S.A.; Perlotti, C.; Sironi, G.; Manfredi, M.T. Bovine Besnoitiosis in an Endemically Infected Dairy Cattle Herd in Italy: Serological and Clinical Observations, Risk Factors, and Effects on Reproductive and Productive Performances. Parasitol. Res. 2019, 118, 3459–3468. [Google Scholar] [CrossRef] [PubMed]
- Waap, H.; Nunes, T.; Cortes, H.; Leitão, A.; Vaz, Y. Prevalence and Geographic Distribution of Besnoitia Besnoiti Infection in Cattle Herds in Portugal. Parasitol. Res. 2014, 113, 3703–3711. [Google Scholar] [CrossRef] [PubMed]
- Reis, Y.; Cortes, H.; Viseu Melo, L.; Fazendeiro, I.; Leitão, A.; Soares, H. Microtubule Cytoskeleton Behavior in the Initial Steps of Host Cell Invasion by Besnoitia Besnoiti. FEBS Lett. 2006, 580, 4673–4682. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shkap, V.; Reske, A.; Pipano, E.; Fish, L.; Baszler, T. Immunological Relationship between Neospora Caninum and Besnoitia Besnoiti. Vet. Parasitol. 2002, 106, 35–43. [Google Scholar] [CrossRef]
- Hornok, S.; Fedák, A.; Baska, F.; Basso, W.; Dencso, L.; Tóth, G.; Szeredi, L.; Abonyi, T.; Dénes, B. Vector-Borne Transmission of Besnoitia Besnoiti by Blood-Sucking and Secretophagous Flies: Epidemiological and Clinicopathological Implications. Parasites Vectors 2015, 8, 4–9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Álvarez-García, G.; Fernández-García, A.; Gutiérrez-Expósito, D.; Quiteria, J.A.R.S.; Aguado-Martínez, A.; Ortega-Mora, L.M. Seroprevalence of Besnoitia Besnoiti Infection and Associated Risk Factors in Cattle from an Endemic Region in Europe. Vet. J. 2014, 200, 328–331. [Google Scholar] [CrossRef] [PubMed]
- Garrido-Castañé, I.; Romero, A.O.; Espuny, J.C.; Hentrich, B.; Basso, W. Besnoitia Besnoiti Seroprevalence in Beef, Dairy and Bullfighting Cattle in Catalonia (North-Eastern Spain): A Cross-Sectional Study. Parasitol. Int. 2019, 69, 71–74. [Google Scholar] [CrossRef]
- Esteban-Gil, A.; Calvete, C.; Casasús, I.; Sanz, A.; Ferrer, J.; Peris, M.P.; Marcén-Seral, J.M.; Castillo, J.A. Epidemiological Patterns of Bovine Besnoitiosis in an Endemic Beef Cattle Herd Reared under Extensive Conditions. Vet. Parasitol. 2017, 236, 14–21. [Google Scholar] [CrossRef]
- Schares, G.; Langenmayer, M.C.; Majzoub-Altweck, M.; Scharr, J.C.; Gentile, A.; Maksimov, A.; Schares, S.; Conraths, F.J.; Gollnick, N.S. Naturally Acquired Bovine Besnoitiosis: Differential Distribution of Parasites in the Skin of Chronically Infected Cattle. Vet. Parasitol. 2016, 216, 101–107. [Google Scholar] [CrossRef]
- Frey, C.F.; Gutiérrez-Expósito, D.; Ortega-Mora, L.M.; Benavides, J.; Marcén, J.M.; Castillo, J.A.; Casasús, I.; Sanz, A.; García-Lunar, P.; Esteban-Gil, A.; et al. Chronic Bovine Besnoitiosis: Intra-Organ Parasite Distribution, Parasite Loads and Parasite-Associated Lesions in Subclinical Cases. Vet. Parasitol. 2013, 197, 95–103. [Google Scholar] [CrossRef]
- Schares, G.; Basso, W.; Majzoub, M.; Rostaher, A.; Scharr, J.C.; Langenmayer, M.C.; Selmair, J.; Dubey, J.P.; Cortes, H.C.; Conraths, F.J.; et al. Comparative Evaluation of Immunofluorescent Antibody and New Immunoblot Tests for the Specific Detection of Antibodies against Besnoitia Besnoiti Tachyzoites and Bradyzoites in Bovine Sera. Vet. Parasitol. 2010, 171, 32–40. [Google Scholar] [CrossRef] [PubMed]
- Grisez, C.; Bottari, L.; Prévot, F.; Alzieu, J.P.; Liénard, E.; Corbière, F.; Rameil, M.; Desclaux, X.; Lacz, C.; Boulon, C.; et al. Real-Time PCR on Skin Biopsies for Super-Spreaders’ Detection in Bovine Besnoitiosis. Parasites Vectors 2020, 13, 529. [Google Scholar] [CrossRef] [PubMed]
Variable | Category | Number | IFAT+ | (%) | OR | p |
---|---|---|---|---|---|---|
Age (years) | 1 | 34 | 7 | 20.6 | Continuous 0.837 | 0.394 |
2 | 72 | 40 | 55.6 | |||
3 | 49 | 33 | 67.3 | |||
4 | 47 | 28 | 59.6 | |||
5 | 39 | 19 | 65.5 | |||
6 | 13 | 9 | 69.2 | |||
7 | 14 | 9 | 64.3 | |||
8 | 4 | 3 | 75.0 | |||
Total | 262 | 148 | 56.5 | |||
Time on herd (years) | <1 | 47 | 18 | 38.3 | Continuous 1.683 | <0.05 |
1 | 34 | 7 | 20.6 | |||
2 | 75 | 43 | 57.3 | |||
3 | 43 | 29 | 67.4 | |||
4 | 21 | 15 | 71.4 | |||
5 | 20 | 18 | 90.0 | |||
6 | 12 | 9 | 75.0 | |||
7 | 7 | 6 | 85.7 | |||
8 | 3 | 3 | 100.0 | |||
Total | 262 | 148 | 56.5 | |||
Animal’s origin | Study farm | 206 | 124 | 60.2 | reference 1.860 | 0.494 |
Outside farms | 56 | 24 | 42.9 | |||
Total | 262 | 148 | 56.5 | |||
Stage of lactation | Mid lactation | 112 | 67 | 59.8 | reference 1.426 1.015 0.505 0.994 0.232 | 0.373 0.984 0.111 0.988 <0.05 |
Late lactation | 46 | 32 | 69.6 | |||
Dry period | 10 | 6 | 60.0 | |||
Postpartum | 33 | 15 | 45.5 | |||
Peak lactation | 38 | 23 | 60.5 | |||
Heifer | 23 | 5 | 21.7 | |||
Total | 262 | 148 | 56.5 |
Variable | Group | Number | Mean (σ) | Min. | Max. | Estimated | p | |
---|---|---|---|---|---|---|---|---|
Milk somatic cell count (×1000 cells/mL) | Seronegative | 96 | 189 | (266) | 18 | 1889 | reference 139.63 | <0.05 |
Seropositive | 143 | 300 | (611) | 10 | 5038 | |||
Total | 239 | 255 | (505) | 10 | 5038 | |||
Daily milk production (kg) | Seronegative | 96 | 34.0 | (8.7) | 10.3 | 56.8 | reference 1.08 | 0.280 |
Seropositive | 143 | 34.9 | (8.2) | 15.2 | 56.6 | |||
Total | 239 | 34.6 | (8.4) | 10.3 | 56.8 | |||
305-mature equivalent milk yield (kg) | Seronegative | 96 | 10,403 | (1635) | 5866 | 14,802 | reference −62.6 | 0.767 |
Seropositive | 143 | 10,710 | (1674) | 7487 | 15,613 | |||
Total | 239 | 10,587 | (1665) | 5866 | 15,613 | |||
Milk protein content (%) | Seronegative | 96 | 3.37 | (0.29) | 2.69 | 4.02 | reference −0.01 | 0.910 |
Seropositive | 143 | 3.38 | (0.34) | 2.62 | 4.56 | |||
Total | 239 | 3.38 | (0.32) | 2.62 | 4.56 | |||
Milk fat content (%) | Seronegative | 96 | 4.38 | (0.86) | 1.97 | 7.62 | reference 0.17 | 0.126 |
Seropositive | 143 | 4.48 | (0.86) | 2.28 | 6.72 | |||
Total | 239 | 4.44 | (0.86) | 1.97 | 7.62 | |||
Calving interval | Seronegative | 59 | 434 | (98) | 324 | 885 | reference 1.86 | 0.916 |
Seropositive | 103 | 438 | (106) | 323 | 912 | |||
Total | 162 | 436 | (103) | 323 | 912 | |||
Number of inseminations | Seronegative | 61 | 2.8 | (1.8) | 1 | 8 | reference 0.14 | 0.655 |
Seropositive | 110 | 2.9 | (2.0) | 1 | 10 | |||
Total | 171 | 2.8 | (1.9) | 1 | 10 |
Variable | Group | Number | Mean (σ) | Min. | Max. | Estimated | p | |
---|---|---|---|---|---|---|---|---|
Milk somatic cell count (×1000 cells/mL) | Without cysts | 50 | 141 | (141) | 20.3 | 712 | reference 304.27 | <0.05 |
Sclerocysts | 46 | 370 | (820) | 14 | 5038 | |||
Total | 90 | 252 | (590) | 14 | 5038 | |||
Daily milk production (kg) | Without cysts | 50 | 35.4 | (6.4) | 20.8 | 50.4 | reference 1.65 | 0.261 |
Sclerocysts | 46 | 37.4 | (8.7) | 15.2 | 56.8 | |||
Total | 90 | 36.4 | (7.6) | 15.2 | 56.8 | |||
305-mature equivalent milk yield (kg) | Without cysts | 50 | 10,306 | (1244) | 7949 | 13,604 | reference 316.8 | 0.296 |
Sclerocysts | 46 | 10,982 | (7815) | 7815 | 14,433 | |||
Total | 90 | 10,633 | (1516) | 7815 | 14,433 | |||
Milk protein content (%) | Without cysts | 50 | 3.33 | (0.27) | 2.62 | 4.02 | reference 0.04 | 0.487 |
Sclerocysts | 46 | 3.35 | (2.72) | 2.72 | 4.16 | |||
Total | 90 | 3.34 | (0.29) | 2.62 | 4.16 | |||
Milk fat content (%) | Without cysts | 50 | 4.59 | (0.81) | 2.46 | 6.65 | reference 0.11 | 0.480 |
Sclerocysts | 46 | 4.64 | (3.10) | 3.11 | 6.72 | |||
Total | 90 | 4.61 | (0.82) | 2.46 | 6.72 | |||
Calving interval | Without cysts | 50 | 403 | (70) | 326 | 584 | reference 17.77 | 0.350 |
Sclerocysts | 46 | 423 | (79) | 328 | 607 | |||
Total | 90 | 413 | (75) | 326 | 607 | |||
Number of inseminations | Without cysts | 50 | 2.3 | (1.8) | 1 | 8 | reference 0.15 | 0.700 |
Sclerocysts | 46 | 2.6 | (1.6) | 1 | 7 | |||
Total | 90 | 2.5 | (1.7) | 1 | 8 |
Variable | Group | Number | Mean (σ) | Min. | Max. | Estimated | p | |
---|---|---|---|---|---|---|---|---|
Milk somatic cell count (×1000 cells/mL) | Without lesions | 195 | 222 | (483) | 11 | 5038 | reference 113.16 | 0.395 |
Skin lesions | 16 | 319 | (517) | 14 | 2223 | |||
Total | 211 | 230 | (488) | 11 | 5038 | |||
Daily milk production (kg) | Without lesions | 195 | 35.0 | (8.0) | 10.3 | 56.6 | reference 0.01 | 0.997 |
Skin lesions | 16 | 36.9 | (9.4) | 23.4 | 56.8 | |||
Total | 211 | 35.2 | (8.2) | 10.3 | 56.8 | |||
305-mature equivalent milk yield (kg) | Without lesions | 195 | 10,629 | (1598) | 6267 | 15,613 | reference −605.0 | 0.134 |
Skin lesions | 16 | 10,555 | (1834) | 7815 | 14,433 | |||
Total | 211 | 10,622 | (1619) | 6267 | 15,613 | |||
Milk protein content (%) | Without lesions | 195 | 3.37 | (0.30) | 2.62 | 4.43 | reference 0.01 | 0.896 |
Skin lesions | 16 | 3.30 | (026) | 2.77 | 3.86 | |||
Total | 211 | 3.36 | (0.30) | 2.62 | 4.43 | |||
Milk fat content (%) | Without lesions | 195 | 4.44 | (0.87) | 1.97 | 7.62 | reference 0.13 | 0.550 |
Skin lesions | 16 | 4.62 | (0.83) | 0.83 | 6.16 | |||
Total | 211 | 4.46 | (0.86) | 1.97 | 7.62 | |||
Calving interval | Without lesions | 195 | 431 | (96) | 324 | 912 | reference −69.35 | <0.05 |
Skin lesions | 16 | 365 | (31) | 332 | 424 | |||
Total | 211 | 425 | (94) | 324 | 912 | |||
Number of inseminations | Without lesions | 195 | 2.7 | (1.8) | 1 | 10 | reference −1.08 | 0.061 |
Skin lesions | 16 | 1.6 | (0.9) | 1 | 3 | |||
Total | 211 | 2.6 | (1.8) | 1 | 10 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Anastácio, C.; Bexiga, R.; Nolasco, S.; Zúquete, S.; Delgado, I.L.S.; Nunes, T.; Leitão, A. Impact of Endemic Besnoitiosis on the Performance of a Dairy Cattle Herd. Animals 2022, 12, 1291. https://doi.org/10.3390/ani12101291
Anastácio C, Bexiga R, Nolasco S, Zúquete S, Delgado ILS, Nunes T, Leitão A. Impact of Endemic Besnoitiosis on the Performance of a Dairy Cattle Herd. Animals. 2022; 12(10):1291. https://doi.org/10.3390/ani12101291
Chicago/Turabian StyleAnastácio, Catarina, Ricardo Bexiga, Sofia Nolasco, Sara Zúquete, Inês L. S. Delgado, Telmo Nunes, and Alexandre Leitão. 2022. "Impact of Endemic Besnoitiosis on the Performance of a Dairy Cattle Herd" Animals 12, no. 10: 1291. https://doi.org/10.3390/ani12101291
APA StyleAnastácio, C., Bexiga, R., Nolasco, S., Zúquete, S., Delgado, I. L. S., Nunes, T., & Leitão, A. (2022). Impact of Endemic Besnoitiosis on the Performance of a Dairy Cattle Herd. Animals, 12(10), 1291. https://doi.org/10.3390/ani12101291